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Diversification Rates of the & ORIGINAL ARTICLE doi:10.1111/evo.13511 Diversification rates of the “Old Endemic” murine rodents of Luzon Island, Philippines are inconsistent with incumbency effects and ecological opportunity Dakota M. Rowsey,1,2,3 Lawrence R. Heaney,4 and Sharon A. Jansa1,2 1Bell Museum of Natural History, University of Minnesota, St. Paul, Minnesota 55108 2Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, Minnesota 55108 3E-mail: [email protected] 4Field Museum of Natural History, 1400 S Lake Shore Drive, Chicago, Illinois 60605 Received April 9, 2018 Accepted May 18, 2018 Diversity-dependent cladogenesis occurs when a colonizing lineage exhibits increasing interspecific competition as it ecologically diversifies. Repeated colonization of a region by closely related taxa may cause similar effects as species within each lineage com- pete with one another. This may be particularly relevant for secondary colonists, which could experience limited diversification due to competition with earlier, incumbent colonists over evolutionary time. We tested the hypothesis that an incumbent lineage may diminish the diversification of secondary colonists in two speciose clades of Philippine “Old Endemic” murine rodents—Phloeomyini and Chrotomyini—on the relatively old oceanic island of Luzon. Although phylogenetic analyses confirm the independent, non- contemporaneous colonization of Luzon by the ancestors of these two clades, we found no support for arrested diversification in either. Rather, it appears that diversification of both clades resulted from constant-rate processes that were either uniform or favored the secondary colonists (Chrotomyini), depending on the method used. Our results suggest that ecological incumbency has not played an important role in determining lineage diversification among Luzon murines, despite sympatric occurrence by constituent species within each lineage, and a substantial head start for the primary colonists. KEY WORDS: adaptive radiation, Phloeomyini, Chrotomyini, Murinae, oceanic island, systematics. The factors that contribute to species and ecological diversity are genetic context, ecological opportunity may manifest as a pattern of central concern in evolutionary biology. One of the key triggers of diversity-dependent cladogenesis, in which lineage diversifica- shown to contribute to cladogenesis and morphological evolution tion rates decrease as competition for available niches increases is ecological opportunity, or the availability of unoccupied niches during a radiation (Nee et al. 1992; Rabosky and Lovette 2008; for a lineage to diversify into (Schluter 2000a; Yoder et al. 2010). Skipwith et al. 2016). The phylogenetic signature left by this pro- This opportunity can be generated by several factors, including cess can be detected by analyzing the branching patterns of the dispersal to a depauperate ecosystem, such as an oceanic island focal clade using standard diversification rate analyses (Rabosky (Baldwin and Sanderson 1998, Reddy et al. 2012; Borregaard 2006; Rabosky 2014). et al. 2017) or an evolutionary innovation that provides relief The influence of competition in shaping diversity has been from existing competition (Wainwright et al. 2012). Ecological explored for unfolding adaptive radiations in a variety of natural opportunity can facilitate adaptive radiation, rapidly producing a systems, especially islands, and previous studies have provided variety of ecologically and morphologically diverse species (Lack support for its effects on the rate of species accumulation (which 1947; Gillespie 2004; Losos 2011). When examined in a phylo- we refer to as diversification rates) and morphological change over C 2018 The Author(s). Evolution C 2018 The Society for the Study of Evolution. 1420 Evolution 72-7: 1420–1435 DIVERSIFICATION OF LUZON OLD ENDEMIC MURINES time (which we refer to more broadly as phenotypic evolutionary constituent species (Drake 1991). The ability of a lineage to col- rates) (Whittaker and Fernandez-Palacios 2007). For example, onize given the existence of a competitor is dependent on several Schluter and Grant (1983) showed that community assembly of factors, including habitat availability, presence of predators, and Geospiza finches is functionally overdispersed, which minimizes relatedness of invading species to incumbent species (Fukami interspecific competition for limited food resources. In a taxo- 2007; Louette and De Meester 2007; Tan et al. 2012). These nomically broad study, Schluter (2000b) used a meta-analysis short-term ecological effects on community composition, when approach to examine the prevalence of ecological character extended over large temporal scales, may result in differences in displacement, or the divergence in phenotype associated with evolutionary process between primary and secondary colonizing niche differentiation in closely related species, in natural systems. lineages. His results indicated this phenomenon is common and strongly From this macroevolutionary perspective, incumbency ef- supported in taxa such as Gasterosteus sticklebacks, Geospiza fects can be examined in two different types of systems: those finches, and heteromyid rodents of the North American desert that have been released from incumbency effects through extinc- southwest, although direct causal links between interspecific tion of competitors or dispersal to a novel environment, and those competition and phenotypic change were often lacking (Schluter in which lineages come into competition due to secondary col- 2000b). In this regard, Parent and Crespi (2009) determined onization. A popular example of diversification after extinction intraspecific variation in Galapagos´ Bulimulus land-snail shell of a competing lineage is the Cretaceous-Paleogene (K-Pg) ex- shape was negatively correlated with the number of congeners tinction and subsequent ecological release of mammals during occurring in the same habitat type and positively correlated with the Cenozoic (O’Leary et al. 2013, but see dos Reis et al. 2014). food resource heterogeneity. Finally, several recent studies of Similarly, Darwin’s finches provide a classic example of diver- lineages on oceanic islands have detected patterns of lineage sification after dispersal to a competitor-deficient system (Burns diversification consistent with declining ecological opportunity, et al. 2014). In both cases, the focal lineage undergoes rapid di- including Hawaiian leafhoppers (Bennett and O’Grady 2013), versification after existing incumbency effects—in the form of New Caledonian geckos (Skipwith et al. 2016), and Philippine competing lineages—have been removed. Detecting such exam- frogs (Blackburn et al. 2013). In sum, these studies provide ples requires analysis of diversification rates either in the context evidence that resource availability in the absence of competition of a densely sampled fossil record or with a phylogenetic per- can expand the intraspecific variation that may promote the evo- spective that includes both dispersing lineages as well as source lution of ecologically distinct species and thus result in increased taxa. Alternatively, incumbency effects on diversification may lineage diversification as well as morphological evolution. occur when two lineages come into contact through independent Nevertheless, most studies to date have focused on the evolu- colonizations of a system. In this case, we might expect sec- tion of a single lineage and have not addressed how diversification ondary colonists to experience reduced ecological opportunity— is affected when a system contains multiple, ecologically similar, and resulting lower diversification rates—compared to primary radiating lineages. Just as density dependence can slow diversi- colonists. Detecting incumbency effects in this case requires a ro- fication within a single radiating lineage, we can predict that the bust phylogenetic framework for the two interacting clades, along presence of an ecologically similar lineage may reduce the rate with analyses of diversification patterns and rates. In addition, of diversification of a second lineage that disperses to the system. researchers must also make prima facie arguments that the two If the colonizing events were asynchronous, the later-dispersing lineages are ecologically similar enough to potentially compete clade may experience a lower diversification rate proportional to over limited resources. Systems that satisfy these biological and the extent of diversification of the primary lineage at the time of methodological requirements for either approach are relatively secondary colonization. The macroevolutionary advantage held rare, meaning there is much to learn about how incumbency and by this primary colonizing lineage is an example of an incum- ecological release affect diversification. bency effect, whereby a lineage gains an advantage simply by Despite the relative scarcity of studies in which multiple being present in an area first (Case 1991; Alroy 1996). ecologically similar clades have colonized a system, several au- Whereas our study focuses on the role of incumbency at the thors have used this approach to test for incumbency effects at macroevolutionary scale, historically, incumbency (or priority) continental scales in birds, fishes, and mammals, examining both effects were hypothesized as a mechanism to explain alternative rates of lineage diversification (Betancur-R. et al. 2012; Schenk stable states in community assembly. In this context, the presence et al. 2013) and
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